Understanding the mechanical determinants of the energy cost of limb swing is crucial for refining our models of locomotor energetics as well as improving treatments for those suffering from impaired limb-swing mechanics. In this study we use guinea fowl (Numida meleagris) as a model to explore whether mechanical work at the joints explains limb-swing energy use by combining inverse dynamic modeling and muscle-specific energetics from blood flow measurements. We found that the overall efficiency of the limb swing increased markedly from walking (3 %) to fast running (17 %), and are well below the usually accepted maximum efficiency of muscle, except at the fastest speeds recorded. The estimated efficiency of a single muscle used during ankle flexion (tibialis cranialis) parallels that of the total limb-swing efficiency (3 % walking, 15 % fast running). Taken together, these findings do not support the hypothesis that joint work is the major determinant of limb-swing energy use across the animals speed range and warn against making simple predictions of energy use based on joint mechanical work. To understand limb-swing energy use, mechanical functions other than accelerating the limb segments need to be explored, including isometric force production and muscle work arising from active and passive antagonist muscle forces.